MARINE ECOLOGY PROGRESS SERIES
Mar Ecol Prog Ser
Vol. 196: 169-177,2000
Published April 18
Egg production by colonies of a gorgonian coral
Elizabeth A. Beiring*,Howard R. Lasker
Department of Biological Sciences. University a t Buffalo, Buffalo, New York 14260, USA
ABSTRACT: Reproductive success, the production and fertilization of gametes, is a key component of
fitness Among many colonial marine invertebrates, the production of gametes by a colony is a function
of both gamete production per module (e.g.,polyp, zooid) and the number of modules in the colony
(i.e., colony size). We examined variance in gamete production per polyp and egg production per
colony over a range of colony sizes, and the relationship between egg production and growth m the
common Caribbean gorgonian Plexaura flexuosa. The number of polyps per colony and the average
number of mature eggs per polyp both were greater among larger female colonies (>70 cm in height)
than among smalIer colonies (c70cm), resulting in a 1 to 2 order of magnitude increase in whole colony
egg release for the larger colonies. In a group of 24 colonies, 98 % of the 9.2 X 106 eggs produced in one
spawning event came from the 12 colonies taller than 70 cm. Branch extension rates showed no relationship to colony size, but whole colony relative growth appears to decrease as colony size increases.
This suggests that proportionately less energy is used for growth as a colony gets larger, and thus may
be available for reproduction.
K E Y WORDS: Reproduction . Growth . Invertebrates . Modular animals . Plexaura flexuosa
INTRODUCTION
An array of studies has examined the reproductive
biology of benthic marine invertebrates in the context
of life history strategies (e.g., Vance 1973, Harvell &
Grosberg 1988, Levitan 1995).Factors such as fertilization success and larval mortality have been considered
important determinants of reproductive success (i.e.,
the production and fertilization of gametes). However,
for the many marine invertebrates that exhibit clonal
growth, the highly variable size of mature colonies can
also lead to large differences in numbers of gametes
produced. This in turn can have a tremendous effect
on estimates of reproductive success among colonies
and populations. To date, only a few studies have estimated egg production of whole colonies, and they
have noted high levels of variance based on colony size
(e.g., Babcock 1984, 1991, Coma et al. 1995, Hall &
Hughes 1996). Variance in gamete production among
'Present address: Office of Wetlands, Oceans, and Watersheds (4504F),U.S. Environmental Protection Agency, Ariel
Rios Building, 1200 Pennsylvania Ave. NW, Washington, DC
20460, USA. E-mail: [email protected]
Q Inter-Research 2000
Resale of full article not permitted
colonies can decrease effective population size because effective population size is inversely proportional to variance in reproductive success (e.g.,
Hughes et al. 1992). Furthermore, 2 studies have indicated that large colonies contribute disproportionately
to egg production by whole populations (Babcock
1984, Coma et al. 1995).
Variance in the reproductive output of clonal taxa is
primarily a function of the iterative production of modules, each of which may be capable of reproduction.
Additional variability is associated w ~ t hthe integration
of modules into physiologically connected colonies. For
example, in many corals and other colonial animals all
modules in a colony delay reproduction until the
colony reaches a minimum size (e.g., Karlson 1986,
Harvell & Crosberg 1988, Coma et al. 1995). Additionally, gamete production per polyp increases as colony
size increases among some coral species (e.g.,Babcock
1991, Coma et al. 1995, Hall & Hughes 1996). Delay in
reproduction and increases in egg production per
polyp with colony size may reflect greater availability
of energy in general among larger colonies or a change
in the allocation of energy from growth to reproduction
(e.g., Hughes & Jackson 1985, Kinzie & Sarmiento
Mar Ecol Prog Ser 196: 169-177, 2000
pared the relative contributions of colonies of various
sizes to egg production by a population. Using measurements of branch extension and estimates of relative growth in whole colonies over a range of colony
heights, we (5) examined the relationship between
reproductive output and growth. Although we present
data on the timing of both egg and spermary development, most of our discussion about reproductive output
focuses on egg production. Eggs are more readily
quantified than sperm, and although sperm density
sometimes limits gorgonian reproductive success (Lasker et al. 1996), the number of eggs produced sets an
upper limit for reproductive success.
1986, Hall & Hughes 1996). Thus life history analyses
of clonal organisms should incorporate data on the
fecundity of modules and colonies, as well as the manner in which resources are distributed between fecundity and growth of the colonies.
The objectives of this study were (1)to document the
reproductive cycle of Plexaura flexuosa, a common
Caribbean gorgonian coral, and (2) to examine variance in gamete volume per polyp, egg production by
whole colonies, and growth of branches and colonies.
Using measurements of egg production per polyp,
polyp density, and colony surface area within and
across colonies, we (3) quantified the relationship between colony size and egg production, and (4) com-
MATERIALS AND METHODS
2
May
June
~Es 0
July
0
0
0
-
P
"
/0/
$ ? ? q , S
0
$.-"
++
.I
7
W
+
Days After Full Moon
Fig.1. PIexawa CIex~lose.
Average gamete volume (mm3)
per polyp (+SE}
over 5 lunar cycles of the 1994 reproductive season for (A) 6 male and
(B)6 female colonies. Samples were taken on all dates labeled. Full
moons were May 25, June 25, July 22,August 21, end September 19
We assessed reproductive output and
growth of Plexaura flexuosa colonies on
patch reefs in the San Blas Islands, Panama.
P. flexuosa is a gonochoric branching gorgonian coral common throughout the Caribbean (Bayer 1961, Goldberg 1973, Lasker
& Coffroth 1983). Unless otherwise stated,
all samples were collected from colonies on
Korbiski Reef, a patch reef 2 to 4 m deep
(Korbiski-l in Robertson 1987, Fig. 1). All
P. flexuosa samples were preserved in 10 %
formalin in seawater immediately after collection, then rinsed in freshwater for -16 h
and transferred to 70% ethanol before examination.
Reproductive cycle. A number of plexaurids, including Pseudoplexaura spp., Plexaurella sp., and the congeners Plexaura homomalla and Plexaura kuna, spawn shortly
after the summer full moons (Brazeau &
Lasker 1989, Coma & Lasker 1997, pers.
obs.). In order to determine the spawning
cycle of Plexaura flexuosa, gamete volumes
in polyps from 6 male and 6 female colonies
were followed over 5 lunar cycles during the
1994 summer. One growing tip (i.e., 1"
branch) from each colony was taken approximately biweekly from May 29, 1994 to
October 3, 1994, and more frequently (every
3 to 4 d) during July and August when we
suspected spawning would occur.
Average gamete volume per polyp for each
branch was determined by counting and
measuring the diameters of all eggs (or spermanes) m 10 polyps uslng a binocular dlsSetting microscope fitted with an eyepiece
micrometer. Polyps were chosen randomly
from a segment of the branch between 2 and
Beiring & Lasker: Whole colony egg production
3 cm from the branch tip. Gamete diameters were converted to volumes (assuming gametes were spherical),
summed within each polyp, then averaged over the
10 polyps in each sample. Eggs were pink and up to
-750 pm in diameter; spermaries were gray to beige,
and up to -450 pm in diameter. Female polyps seldom contained more than 4 large (1400 pm) eggs, while
male polyps contained as many as 22 spermaries.
Variability in egg production. Egg production by a
polyp may vary depending on the polyp's location
within a colony or on the size of the colony itself. To
examine within-colony variability, average egg volume per polyp was determined for branches at different distances from the branch tips. Branches were classified according to branch order (sensu Brazeau &
Lasker 1988), and 10 polyps were dissected from the
central 1 cm portion of 1" source, l " tributary, 2" and 3"
branches, and from pieces of the colony base. One
branch of each type was sampled from each of 8 female
colonies (50 to 81 cm tall). Samples were collected 1 to
2 d after the July 1994 full moon (-4 to 5 d before
spawning). Egg volume data were heteroscedastic and
could not be transformed to normality; therefore differences among branch orders were tested using Friedman's 2-way (colony X branch order) ANOVA by ranks.
To examine variability in egg production per polyp
among colonies of different sizes, one 1" branch was
taken from each of 24 female colonies ranging from 33
to 107 cm in height. Samples were collected 4 to 5 d
before the July 1994 full moon (-10 to 11 d before
spawning). Egg volume per polyp for each branch was
determined by counting and measuring all eggs in 10
polyps, converting egg diameters to volumes, summing the egg volumes within each polyp, then averaging the total volume across the 10 polyps. Polyps were
chosen randomly from a segment of the branch between 2 and 3 cm from the branch tip. Regression
analysis was used to test the relationship between egg
volume per polyp and colony height.
Release of eggs. The total number of eggs released
during a spawning event was calculated for 24
female colonies using counts of mature eggs per
polyp, estimates of the percent of mature eggs released per spawning event, and estimates of the
number of polyps per colony of a given size, as described below.
Size and number of mature eggs per polyp: To determine the size of mature eggs (i.e., those that could
be spawned), 1 clump of primary and secondary
branches was collected from each of 2 female colonies
and kept in separate running-seawater aquaria during
the August 1995 spawning. Over 200 eggs spawned
from these branches on August 19 and 20 were collected, preserved in 5 % formalin, and their diameters
measured.
171
The average number of mature eggs per polyp was
determined for primary branches from 24 female
colonies ranging from 33 to 107 cm tall (see 'Variability
in egg production' above). Because these samples
were collected -10 to 11 d before spawning, eggs had
not yet reached their maximum size. To correct for this,
a comparison was made of egg sizes from branches of
6 colonies collected -10 and - 3 d before spawning
(10 polyps per colony per sampling event).
Eggs released during spawning: The percent of
mature eggs released during a spawning event was
estimated by comparing the average number of mature
eggs per polyp in branches that were collected from 6
female colonies before and after spawning events in
both July and August 1994 (1 branch per colony per
sampling event; 10 polyps per branch). Samples for
'before spawning' were collected 0 to 5 d after the full
moon. Samples for 'after spawning' were collected 15
to 17 d after the full moon.
Polyps per colony: Polyp densities on branches of 8
female colonies (50 to 81 cm tall) were determined
from counts of the number of polyps within measured
areas of 5 branch orders ( l 0source, 1" tributary, 2' and
3" branches, and a piece from the colony base). For l",
2", and 3" branches, the measured areas were approximately 1 cm long and located at the center of each
branch; branch diameter at the ends of the 1 cm section
was measured and surface area computed using the
average diameter (range for all branches was 0.99 to
2.26 cm2). Polyp density within an area of approximately l X 2 cm (range 1.64 to 3.33 cm2)was measured
at the base of the colony. Polyp densities were compared using a 2-way ANOVA without replication.
In order to estimate the number of polyps in an entire
colony, the polyp density measures were multiplied by
the total surface area of branches of each order. Total
surface areas for the different branch orders were estimated for 10 colonies (33 to 107 cm in height) from
Tiantupo Reef (Tiantupo-l in Robertson 1987). All
branches on each colony were counted and categorized by branch order. Length (to nearest mm using a
flexible clear ruler) and diameter (to nearest 0.1 mm
using calipers) were measured on ten l " , 2', and 3"
branches and on all higher order branches. Surface
area (SA, cm2) of each branch was calculated (ndh).
Average SA and polyp density for each branch order
were used to calculate whole colony polyp number.
For purposes of prediction, a regression was fitted
between number of polyps and colony volume (i.e.,the
volume of a box fitted around the colony calculated
from colony maximum height, width, and depth measured to nearest cm) for these 10 colonies. Because this
relationship was highly significant, the resulting regression equation was used to estimate the number of
polyps on another group of 24 female colonies using
Mar Ecol Prog Ser 196: 169-177, 2000
4
Base
3'
Base
Branch Order
Colony Height (cm)
Fig. 2. Plexaura flexuosa. Average egg volume (mm3) per
polyp (*SE) across 5 branch orders in 8 colonies (10 polyps
per branch order per colony). S: source, T: tributary
Fig. 3. Plexaura flexuosa. Average egg volume (mm3) per
polyp as a function of colony height in 24 colonies (10 polyps
per colony)
measurements of their volume (i.e., height X width X
depth). The number of eggs released during spawning
by each of the 24 colonies was estimated by multiplying (1) the number of polyps in the colony by (2) the
number of mature eggs produced per polyp by (3) the
percentage of mature eggs in a polyp released during
a spawning event.
Growth rates. Growth rates were determined for 29
colonies on 3 patch reefs (Tiantupo-l, Porvenir-17, and
Aguadargana-l in Robertson 1987). Our measure of
growth was the change in length of primary branches.
On each colony, a section of 11 to 21 primary branches
was identified and sketched to allow relocation. The
length of each primary branch was measured (+ 1 mm)
in 1995 and again in 1996 (297 to 355 d). Because the
branches measured on each colony were adjacent to
one another, their growth rates may not have been
independent. Therefore, we used averages for each
colony in our statistical analyses.
Changes in the average number of mature eggs
(2500 pm; see below) per polyp over time showed that
5 of the 6 females spawned heavily during only 1 or 2
lunar cycles (after the July and/or August full moons;
results not shown), in contrast to the male colonies,
each of which spawned 4 or 5 times over the 5 lunar
cycles.
Our sampling scheme was based on our familiarity
with the spawning of other plexaurids, and it is possible that Plexaura flexuosa spawned outside of our
summer sampling period. However, the shape of the
egg volume per polyp curve (Fig. lB), with its peak in
July, indicates that there is seasonality to P. flexuosa
spawning, and that if spawning occurs outside this
time period, it 1s likely to be light. Furthermore, average egg volumes of samples taken on February 2,1995
(4 d before the full moon), were similar to those of postspawning samples from October 3, 1994, again suggesting that spawning did not occur outside the summer months.
RESULTS
Variability in egg production per polyp
Reproductive cycle
Plexaura flexuosa spawning events during the summer of 1994 can be identified by precipitous drops in
gamete volume per polyp that occurred after the full
moons (Fig 1). Evidence of spawning was particularly
striking among male colonies (Fig. 1A). All 6 male
colonies spawned after the June 23, July 22, August 21,
and September l?, 1994, full moons. Four of the 6 males
also may have spawned after the May 25 full moon.
Fine-scalesampling after the July 22 and August 21 full
moons indicated that spawning started 6 or 7 d after the
full moon and ended 11 to 15 d after the full moon.
There was no significant difference in average egg
volume per polyp among l", 2", and 3" branches
(Fig. 2; Friedman's X2 = 4.95; p = 0.176). There was
a virtual absence of gametes in polyps from the bases
of colonies, however, which resulted in a significant
difference when these samples were included in the
analysis (Fig. 2; Friedman's X2 = 19.3;p = 0.0007).
Colony height had a significant effect on egg volume
per polyp (Fig. 3; r2 = 0.406; F,.22 = 15.1;p = 0.0008).Although every polyp examined except 1 contained at least
1 egg, there were differences in the percentage of polyps
bringing eggs to maturity. Of the 120 polyps examined
Beiring K Lasker: Whole colony egg production
173
W
+
a
X
o
a
2.5
2.0
-10 d before spawning
-1 d before spawning
L
a,
1.5
0,
m
1.0
0
L
a,
o
5
0.5
0.0
0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0
~
~
C
U
~
O
U
~
N
W
O
~
- - N N @ J m O q V U m O W W W b
~
N
W
O
~
~
N
Fig. 4. Plexaura flexuosa. Comparison of egg size class distributions in 6 colonies -10 and -1 d before spawning (10 polyps
per colony per sampling date)
from the 12 small colonies (<70cm), only 13% contained
large (2400 pm) eggs, with an average of 1.3 large eggs
per polyp among these polyps. Of the 120 polyps from
the 12 large colonies (>70 cm), 55 % contained at least
1 large egg, with an average of 1.9 polyp-'.
Release of eggs
Size and number of mature eggs per polyp
Spawned eggs ranged in size from 533 to 667 pm in
diameter, with an average of 597 27 pm (+SD). A
comparison of egg sizes from -10 and -1 d before
spawning in 6 female colonies showed that the number
of eggs 2400 pm on the earlier date roughly corresponded to the number of eggs 1500 pm on the later
date (Fig. 4). Therefore, for samples collected -10 d
before spawning, we counted all eggs 2400 pm as
'mature eggs' that could be released that month. The
number of mature eggs per polyp in samples from 24
colonies collected -10 d before spawning ranged from
0 to 2.2, and increased with increasing colony size
(Fig. 5A).
*
Eggs released during spawning
Branches collected prior to spawning contained an
average of 1.09 + 0.73 mature eggs per polyp (*SD;
range among branches 0.1 to 2.6; data not shown).
Branches collected after spawning had an average of
0.17 + 0.24 mature eggs per polyp (kSD; range 0.0 to
0.8; data not shown). This observation indicates that
84 % of the mature eggs present in pre-spawning samples were released.
Colony Height (cm)
Fig. 5. Plexaura Ilexuosa. (A) Per polyp fecundity, (B) whole
colony polyp count, and (C) whole colony egg release by
colony height for 24 colonies
Polyps per colony
Total branch counts (all branch orders) of 10 colonies
ranged from 117 branches for a 37 cm tall colony to
3861 branches for a 107 cm tall colony (Table 1). Total
surface area ranged from 0.104 to 6.73 m2 (Table 1).
Pnmary, 2", and 3" branches together accounted for an
average of 92 % of total colony surface area (range 87
to 97 %; Table 1).
Polyp density did not differ across branch orders
(ANOVA without replication, F4,28
= 2.36, p = 0.078) and
averaged 50 + 8 polyps cm-' (kSD).Using this density,
the total number of polyps per colony ranged from 5.18 X
104 (37 cm tall colony) to 3.36 X 106 (107 cm tall colony; Table 1). Colony volume (colony height X width X
Mar Ecol Prog Ser 196: 169-177, 2000
Table 1 Surface area and polyp number estimates for 10 Plexaura flexuosa colonies. Volume given as colony width X depth X
height. Total number of polyps calculated using 50 polyps cm-' (see text). Total number and % of total surface area given for each
branch order
Colony
1
2
3
4
5
6
7
8
9
10
Height
(cm)
33
37
42
42
52
66
70
85
96
107
Volume
(m3)
0.0203
0.0178
0.0194
0.0464
0.0598
0.247
0.549
0.495
0.288
2.25
Total
branch
length
(cm)
Surface
area
(m2)
Total
no. of
polyps
No. of branches (% of total surface area) for each branch order
861
638
782
1040
1940
6830
6010
7110
3890
36200
0.114
0.104
0.129
0 167
0.307
1.06
1.13
l 28
0.755
6.73
56800
51800
64300
83500
154000
528000
566000
642000
377000
3360000
l0
depth) was a good predictor of total number of polyps (r2
= 0.988; F , , 8= 685; p = 0.0001),yielding the equation:
Polyp number = 1.46
10%olony volume (m3)+ 3960
,,,
'l'
103 (52)
78 (45)
95(51)
171 (42)
173 (65)
760 (52)
506 (61)
540 (61)
444 (51)
2681 (65)
2"
3"
33 (27)
9 (18)
29 (35)
8 (12)
36(27)
9(15)
58 (32) 15 (12)
48 (18) 14 (10)
225 (31) 65 (9)
132 (23) 37 (8)
153 (27) 44 (6)
134 (16) 39 (20)
834 (18) 245 (10)
4"
5'
0
3 (3)
0
2 (7)
0
3(7)
6 (10) 2 (3)
5 (6)
1 (2)
21 (4)
7 (3)
11 (4)
4 (2)
14 (3)
5 (2)
9 (4)
4 (4)
78 (4) 15 (1)
6"
7"
0
0
0
0
0
0
0
0
0
0
3 (1) 1 (0.03)
1 (1)
0
2 (1)
0
2 (4)
0
6 (1) 2 (1)
averaging 1.0 + 2.2 (mean + SDI-a 6-fold difference.
Consequently, whole colony egg release (number of
polyps multiplied by number of mature eggs per polyp)
increased dramatically after colony height reached
70 cm, and ranged from 0 to 1.69 X 106 eggs per colony
per spawning event (Fig. 5C).
Whole colony egg release
Colony volume, and therefore polyp count (estimated using Eq. l ) , rose dramatically after a colony
reached -70 cm in height (Fig. 5B) The average number of polyps in colonies less than 70 cm tall was
104 000 + 58 900 (mean + SD); the average number of
polyps in colonies greater than 70 cm was 852000 i
403 000 (mean * SD) -over an 8-fold increase. Similarly, the number of mature eggs per polyp (Fig. 5A)
increased in colonies greater than 70 cm, with colonies
less than 70 cm averaging 0.18 + 0.30 mature eggs per
polyp (mean + SD), and colonies greater than 70 cm
Colony Height (cm)
~rowih
(+ S E )
Fig, 6, Plexdi~rd flexuosa, Average branch growth rate
(mm yr 'l by colony height tor 29 colonies on 3 reefs and
average growth rdte per reef (+SE)
Growth rates
Average branch growth rates varied trenlendously
among colonies, ranging from -13.3 to +37.3 mm yr-'
(Fig. 6). Negative growth rates reflect loss of tissue,
most likely due to predation by the gastropods
Cyphorna spp. and the polychaete Hermodice carunculata. (Plexaura flexuosa is not known to fragment
like its congener P, kuna [pers. obs.].)There was no
relationship between colony size and branch growth
rate (Tiantupo: r2 = 0.198, F = 1.97, p = 0.20; Porvenir17: r2 = 0.007, F = 0.056, p = 0.82; Aguadargana: r2 =
0.028, F = 0.204, p = 0.67).There also was no difference
in branch growth rate among the 3 reefs
= 0.506;
p = 0.61). Branch growth rate across all colonies was
7.7 * 3.4 mm y r ' (average i SE).
As in other gorgonians (Coma 1994), most growth in
Plexaura flexuosa probably occurs in 1" branches.
Because there appears to be no difference in 1" branch
growth rate across colony size for P. flexuosa, the
number of 1" branches divided by total linear length of
a colony represents its relative growth rate. Plotting
this ratio against colony height for the 10 colonies in
Table 1 shows that there are significantly fewer growheight
ing tips per linear cm Of
tissue as
increases (Fig. 7; r = -0.636, P = 0.049). Assuming
that there are no systematic differences in 1" branch
1.75
Beinng & Lasker Whole colony egg production
growth rates throughout a colony (but see Kim 1996),
relative growth decreases as colonies get larger.
DISCUSSION
Colony size and consequences for populations
Large Plexaura flexuosa colonies (>70 cm in height)
produced on average 6 times more mature eggs per
polyp than smaller colonies (Fig. 5A), and they had on
average 8 times more polyps than smaller colonies
(Fig. 5B). These differences in colony size and egg production per polyp resulted in a dramatic increase in
whole colony egg release for colonies over 70 cm tall
(Fig. 5C). Among colonies with mature eggs, those that
were 33 to 66 cm tall released 103 to 104 eggs per
colony per spawning event, while those that were 73 to
107 cm tall released 10' to 106 eggs per colony per
spawning event. Of the estimated 9.2 X 106 eggs
released by these 24 females during 1 spawning event,
9.0 X 106 came from the 12 colonies over 70 cm tall. In
other words, 98% of the eggs were produced by only
half of the colonies.
On 3 other reefs in the San Blas region, female
colonies taller than 70 cm comprised 23,38, and 49 % of
the female populations (Beiring 1997). Using average
colony egg production values from the 24 colonies discussed above (15500 eggs for colonies <70 cm and
749000 eggs for larger colonies), large colonies produce 93 to 98% of the eggs released on these 3 reefs.
Therefore, the vast majority of eggs from these reefs are
produced by a relatively small subset of the population.
In the 2 other studies where whole population egg
production has been estimated, similar results have
been reported. Coma et al. (1995)found that colonies of
the Mediterranean gorgonian Paramuricea clavata
taller than 40 cm comprised only 3 % of the population
yet contributed approximately 40% of the female gametes and 33 % of the male gametes. For the scleractinian Goniastrea aspera, Babcock (1984) reported that
colonies greater than 6 cm in mean radius comprised
less than 22% of the population but contributed approximately 80% of total annual egg production. Although they did not measure egg production, Potts et
al. (1985)found similar results for living surface area; of
65 colonies of 7 Porites species measured, 50% of the
living surface area came from only 6 colonies.
These results indicate that population size alone,
without reference to colony size structure, may be a
poor predictor of population egg production and reproductive success. The huge variance in egg production
among coral colonies leads to a much lower effective
population size than predicted by a simple census of
colonies (Hughes et al. 1992).
Colony Height (cm)
Fig. 7. Plexaura flexuosa. Relationship between colony height
and the number of l" branches per Linear cm of colony for
10 colonies
Reproduction, growth, and colony size
Reproduction and growth are commonly represented as processes competing for limited resources
(e.g.,Jackson & Hughes 1985).The relationship is considerably more complex among clonal animals, where
clonal growth can enhance reproduction by generating additional reproductive modules.
Delay in reproduction until a minimum colony size is
reached is a trait common to many colonial invertebrates (e.g., Harvell & Grosberg 1988, Brazeau &
Lasker 1989,1990, Keough 1989, Babcock 1991, Soong
& Lang 1992, Van Veghel & Kahmann 1994, Coma et
al. 1995, Fan & Dai 1995, Hall & Hughes 1996; see also
review by Harrison & Wallace 1990). Most Plexaura
flexuosa colonies become reproductive between 20
and 30 cm in height (Beiring 1997). Once reproduction
began, reproductive output of individual P. flexuosa
polyps increased with increasing colony size (Figs. 3 Pr
5A). Similar findings have also been reported among
hard corals (Rinkevich & Loya 1979, Kojis & Quinn
1981, 1985, Babcock 1984, 1991, Van Veghel & Kahmann 1994, Hall & Hughes 1996) and other soft corals
(Brazeau & Lasker 1990, Coma et al. 1995).
The relationship between reproductive output and
growth rate is ambiguous. Absolute linear growth rates
(i.e., branch extension rates) did not change with
colony size (Fig. 6), similar to many other anthozoans
(e.g., Kinzie & Sarmiento 1986. Hughes & Connell
1987, Babcock 1991, Yoshioka & Yoshioka 1991, Coma
1994, Goh & Chou 1995, but see Chornesky & Peters
1987). However, there were fewer growing tips, and
presumably less annual extension, per linear cm of
colony with increasing colony height (Fig. 7), and
therefore, on a relative or per polyp basis, less energy
is invested in growth as a colony gets bigger (Connell
Mar Ecol Prog Ser 196: 169-177, 2000
1973, Hughes & Jackson 1985, Hughes & Connell
1987, Soong & Lang 1992, Hall & Hughes 1996).
It is possible that the delay in reproduction and reduced polyp fecundity in smaller colonies are consequences of greater resource allocation to growth at
smaller sizes (Kojis & Quinn 1981, Szmant 1986, Soong
1993, Ward 1995, Hall & Hughes 1996). Because mortality is invariably greater for smaller coral colonies,
such an allocation would allow colonies to grow
quickly out of the more vulnerable smaller size classes
(e.g.,Connell1973, Hughes & Jackson 1985, Jackson &
Hughes 1985, Babcock 1991). However, less energy
used for growth among large colonies does not necessarily translate into greater resource availability for
reproduction. In branching corals, for instance, there
may be a decrease in energy captured per polyp as a
colony gets larger due to an increased percentage of
interior branches with less access to water-borne nutrients and light (Holloran 1986, Kim & Lasker 1997). It
remains to be determined whether a decrease in relative growth reflects a change in allocation or a decrease in per polyp resource capture.
Acknowledgements. Support for this study was provided by
Lerner Gray and Sigma Xi to E.A.B. and by the National Science Foundation (OCE 9217014) to H.R.L.We thank the Kuna
Nation for pern~issionto work In the San Blas and the Smithsonian Tropical Research Institute for logistical support.
Contributions of D. A. Brazeau, M. A. Coffroth, R. Coma, T. L.
Goulet, T Insalaco, K. Kim, R. Tapia, S. Santos, W. Kapela,
and T. Swain to this study are gratefully acknowledged. This
work was part of the E.A.B.'s doctoral dissertation and does
not necessarily reflect the opinions of the Environmental Protection Agency.
LITERATURE CITED
Babcock RC (1984)Reproduction and distribution of two species of Goniastrea (Scleractinia) from the Great Barrier
Reef Province. Coral Reefs 2:187-195
Babcock RC (1991) Comparative demography of three species
of scleractini.an corals using age- and size-dependent classification. Ecology 61:225-244
Bayer FM (1961) The shallow water octocorallia of the West
Indian region. Nijhoff, The Hague
Beiring EA (1997) Life history and reproductive success of a
broadcast-spawmng gorgonian coral and implications for
conservation biology. PhD thesis, State University of New
York at Buffalo
Brazeau DA, Lasker HR (1988) Inter- and intraspecific variation in gorgonian colony morphology. quantifying branching patterns in arboresrc,nt animals. Coral Reefs 7:
139-143
Brazeau DA, Lasker HR (1989) The reproductive cycle and
spawning in a Caribbean gorgonlan. Biol Bull 176:l-7
Brazeau DA. Lasker HR (1990) Sexual reproduction and
external brooding by the Caribbean gorgonian Briareum
asbestinrlm. Mar Biol 104:465-474
Chornesky EA, Peters EC (1987) Sexual reproduction and
colony growth in the scleractlnian coral Porites astreoides.
Biol Bull 172:161-177
Coma R (1994) Energy budget assessment of two benthic
marine cnidarians. PhD thesis, University of Barcelona
Coma R, Lasker HR (1997) Small-scale heterogeneity of fertilization success in a broadcast spawning octocoral. J Exp
Mar Biol Ecol 214.107-120
Coma R, Zabala M, Gili JM (1995) Sexual reproductive effort
in the Mediterranean gorgonian Pararnuricea clavata. Mar
Ecol Prog Ser 117:185-192
Connell JH (1973) Population ecology of reef-building corals.
In: Jones OA, Endean R (eds) Biology and geology of coral
reefs. Academic Press, New York, p 205-245
Fan TY, Dai CF (1995) Reproductive ecology of the scleractinian coral Echinopora Jamellosa in northern and southern
Taiwan. Mar Biol 123:565-572
Goh NKC, Chou LM (1995) Growth of five species of gorgonians (sub-class Octocorallia) in the sedimented waters of
Singapore. PSZN I: Mar Ecol 16:337-346
Goldberg WM (1973) The ecology of the coral-octocoral communities off the southeast Florida coast: geomorphology,
species composition. and zonation. Bull Mar Sci 23:465-488
Hall VR, Hughes TP (1996) Reproductive strategies of modular organisms: comparative studies of reef-building corals.
Ecology 77:950-963
Harrison PL, Wallace CC (1990) Reproduction, dispersal, and
recruitment of scleractinian corals. In: Dubinsky Z (ed)
Ecosystems of the world. Elsevier, Amsterdam, p 133-207
Harvell CD, Grosberg RK (1988) The timing of sexual maturity in clonal animals. Ecology 69:1855-1864
Holloran MK (1986)The relationship between colony size and
larva production in the reef coral Pocillopora damicornis.
In: Jokiel PL, Richmond RH, Rogers RA (eds) Coral reef
population biology. Hawaii Inst Mar Biol Tech Rep, Honolulu, p 167-169
Hughes TP, Connell JH (1987) Population dynamics based on
size or age? A reef-coral analysis. Am Nat 129:818-829
Hughes TP, Jackson JBC (1985) Population dynamics and life
histones of foliaceous corals. Ecol Monogr 55:141-166
Hughes TP. Ayre D, Connell JH (1992)The evolutionary ecology of corals. Trends Ecol Evol7:292-295
Jackson JBC, Hughes TP (1985) Adaptive strategies of coralreef ~nvertebrates.Am Sci 73:265-274
Karlson RH (1986) Disturbance, colonial fragmentation, and
size-dependent life history variation in two coral reef
cnidarians. Mar Ecol Prog Ser 28:245-249
Keough MJ (1989) Variation in growth rate and reproduction
of the bryozoan Bugula nerjtina. Biol Bull 177:277-286
Kirn K (1996) Patterns and controls of modular growth in gorgonian corals. PhD thesis, State University of New York at
Buffalo
&m K, Lasker HR (1997)Flow-mediated resource competition
in the suspension feeding gorgonian Plexaura homomalla
(Esper).J Exp Mar Biol Ecol215:49-64
ffinzie RA, Sarmiento T (1986) Linear extension rate is independent of colony size in the coral Pocillopora d a r n ~ c o r ~ j s .
Coral Reefs 4: 177-181
Kojis BL, Quinn NJ (1981) Aspects of sexual reproduction and
larval development in the shallow water hermatypic coral,
Goniastrea australensis (Edwards and Haime 1857). Bull
Mar Sci 31:558-573
Kojis BL, Quinn NJ (1985) Puberty in Goniastrea favulus age
or size limited? Proc 5th Intl Coral Reef Congress, Tahiti
4:289-293
Lasker HR. Coffroth MA (1983)Octocoral distributions at Carrie Bow Cay, Belize. Mar Ecol Prog Ser 13:21-28
Lasker HR, Brazeau DA, Calderon J , Coffroth MA, Coma R,
Kirn K (1996) In situ rates of fertilization among broadcast
spawning gorgonian corals. B~olBull 190:45-55
Beinng & Lasker: Whole colony egg production
177
.evitan DR (1995) The ecology of fertilization in freespawning invertebrates. In: McEdward L (ed) Ecology of
marine invertebrate larvae. CRC Press, Boca Raton, FL,
p 123-156
Potts DC, Done TJ, Isdale PJ, Fisk DA (1985) Dominance of a
coral community by the genus Porites (Scleractinia). Mar
Ecol Prog Ser 23:79-84
Rinkevich B. Loya Y (1979) The reproduction of the Red Sea
coral Stylophora pistillata. 11. Synchronization in breeding
and seasonality of planulae sheddng Mar Ecol Prog Ser
1:145-152
Robertson DR (1987) Responses of two coral reef toadfishes
(Batrachoididae) to the demise of their primary prey, the
sea urchin. Copeia 3:637-642
Soong K (1993) Colony size as a species character in massive
reef corals. Coral Reefs 12:77-83
Soong K, Lang J C (1992) Reproductive integration in reef
corals. Biol Bull 183:418-431
Szmant AM (1986) Reproductive ecology of Caribbean reef
corals. Coral Reefs 543-53
Vance RR (1973)On reproductive strategies in marine benthic
invertebrates. Am Nat 107:339-352
Van Veghel M U , Kahmann MEH (1994) Reproductive characteristics of the polymorphic Caribbean reef building
coral Montastrea annularis. 11. Fecundity and colony structure. Mar Ecol Prog Ser 109:221-227
Ward S (1995) Two patterns of energy allocation for growth,
reproduction and lipid storage in the scleractinian coral
Pocillopora damicornis. Coral Reefs 14:87-90
Yoshioka PM. Yoshioka BB (1991) A cornpanson of the survlvorship and growth of shallow-water gorgonian species
of Puerto Rico. Mar Ecol Prog Ser 69:253-260
Editorial responsibility: Ron Karlson (Contributing Editor),
Newark, Delaware, USA
Subm~tted:August 26, 1998; Accepted: September 19, 1999
Proofs received from author(s): March 27, 2000